Temporal changes in the bacterial microbiome of the salivary gland and midgut tissues of Rhipicephalus sanguineus (s.l.) ticks in South Africa

Abstract

Tick-borne bacterial pathogens from animals play a significant role in the (re)emergence of human diseases. Rhipicephalus sanguineus sensu lato, a globally prevalent tick, predominantly parasitises domestic dogs but can also feed on humans. We characterised temporal changes in the bacterial microbiome of the midgut and salivary gland tissues of R. sanguineus s.l. ticks and analysed their potential as reservoirs for pathogenic bacteria. A 16 S microbiome and amplicon sequence variant (ASV) approach was used to study the bacteria present in the tissues of R. sanguineus s.l. ticks collected from dogs in Hluvukani, a village in a rural community in Bushbuckridge, Mpumalanga, South Africa, in 2016, 2017 and 2019. Post processing, we obtained 43,161 total sequence reads which were clustered into ASVs by sample year. The final ASVs dataset consisted of seven genera: Coxiella, Anaplasma, Escherichia/Shigella, Ehrlichia, Borrelia, Rickettsia and Wolbachia. No differences in the microbiome profiles of the MG and SG tissues were noted. Coxiella endosymbionts dominated the microbiome in all years. Anaplasma was first detected in 2017, and an increase in Anaplasma levels was detected in 2019, when compared to 2017. All other genera were present at low levels. With the exclusion of Wolbachia, the other detected genera could have pathogenic potential, highlighting the role that R. sanguineus s.l. might play as a reservoir of pathogens.

Description

DATA AVAILABILITY : The raw microbiome datasets generated during the current study are available in the NCBI SRA (PRJNA1176486, https://www.ncbi.nlm.nih.gov/sra/?term=PRJNA1176486). 16 S sequences reported in this study are available on GenBank under accession numbers: Wolbachia-like endosymbiont: PQ508350. Ehrlichia canis: PQ508351. Borrelia-like: PQ508352. Rickettsiales: PQ508353. Coxiella endosymbiont: PQ508354, PQ508355. Anaplasma centrale: PQ508356, PQ508357, PQ508358, PQ508359, PQ508360, PQ508362, PQ508363, PQ508364, PQ508365, PQ508366. Anaplasma platys: PQ508361. CHANGE HISTORY : 17 June 2025. The original online version of this Article was revised: The Acknowledgments section in the original version of this Article was incomplete. “We acknowledge Luis Neves for verifying the tick identification. We also thank the staff of the Hans Hoheisen Wildlife Research Station for logistical support, environmental monitors, Handry Mathebula and Julia D. Sithole, for assistance in the Bushbuckridge-East community, and the tribal council for allowing us to work in their community. Appreciation is extended to Derek Pouchnik and Mark Wildung from the Genomics Sequencing Core at Washington State University for assistance with microbiome sequencing.” It now reads: "We acknowledge Luis Neves for verifying the tick identifications. We thank the staff of the Hans Hoheisen Research Centre for logistical support, environmental monitors, Handry Mathebula and Julia D. Sithole, for assistance in the Bushbuckridge-East community, and the tribal council for allowing us to work in their community. Appreciation is extended to Derek Pouchnik and Mark Wildung from the Genomics Sequencing Core at Washington State University for assistance with microbiome sequencing. We thank the South African National Research Foundation (NRF) for grants 92739 and 110448, and 109350, NIH NIAID R01AI136832, and the Belgian Directorate General for Development Cooperation Framework FA4 (ITM-DGCD) awarded to Marinda Oosthuizen, as well as the Agricultural Sector Education Training Authority (AgriSETA; BU18UP124-18.2) Scholarship and the Meat Industry Trust for the bursary awarded to Rebecca E. Ackermann. The content is solely the responsibility of the authors and does not necessarily represent the official views of the funding bodies." The original Article has been corrected.

Keywords

Anaplasma, Dogs, Bacterial microbiome, Amplicon sequence variants, 16S rRNA, Coxiella

Sustainable Development Goals

SDG-02: Zero Hunger

Citation

Ackermann, R.E., Gall, C.A., Brayton, K.A. et al. Temporal changes in the bacterial microbiome of the salivary gland and midgut tissues of Rhipicephalus sanguineus (s.l.) ticks in South Africa. Scientific Reports 15, 17434 (2025). https://doi.org/10.1038/s41598-025-99189-0.